Early Neanderthals in contact: The Chibanian (Middle Pleistocene) hominin dentition from Velika Balanica Cave, Southern Serbia.

Neanderthals are Eurasian fossil hominins whose distinctive morphology developed in the southwestern corner of Europe and later spread throughout the continent, reaching Southwest Asia before the Late Pleistocene and spreading into Central Asia by 59-49 ka. The timing, tempo, and route of the Neanderthal movements eastward are poorly documented. The earliest probable evidence of Neanderthals in Asia comes from Karain E Cave (Anatolia, Turkey), dated to 250-200 ka. We present four Chibanian (Middle Pleistocene) hominin specimens, representing at least two individuals, from Velika Balanica Cave (Serbia): a permanent upper third molar (BH-2), a deciduous upper fourth premolar (BH-3) refitted to a poorly preserved maxillary fragment with the permanent first molar in the alveolus (BH-4), and a permanent upper central incisor (BH-5). We provide descriptions of the teeth, as well as a comparative analysis of the well-preserved M1 (BH-4), including assessments of cusp angles, relative occlusal polygon area, relative cusp base areas, two- and three-dimensional enamel thickness, and taurodontism. Morphology of both the occlusal surface and the enamel dentine junction of the M1 indicates that the maxillary fragment and associated dP4 belonged to an early Neanderthal child. The heavily worn I1 and M3 are consistent with the Neanderthal morphology, although they are less distinct taxonomically. These Chibanian remains with provenance from layer 3a are constrained by two thermoluminescence dates: 285 ± 34 ka and 295 ± 74 ka. They represent the earliest current evidence of Neanderthal spread into the Eastern Mediterranean Area. We discuss these findings in light of recent direct evidence for cultural connections between Southwestern Asia and Southeast Europe in the Chibanian.

Connections between the Levant and the Balkans in the late Middle Pleistocene: Archaeological findings from Velika and Mala Balanica Caves (Serbia).

Major changes in the technological, economic, and social behavior of Middle Pleistocene hominins occurred at the onset of the Middle Paleolithic, 400-200 ka. However, until recently it was not possible to establish when, where, and how certain forms of Middle Paleolithic behavior appeared and spread into Southeastern Europe, mainly owing to gaps in the Paleolithic record. Here we report new results of dating, material culture, and the archaeological context of finds from the Balanica Cave Complex in Sicevo (Serbia). Two methods-thermoluminescence and electron spin resonance-were used to date the sequence. The geoarchaeological context was examined through sedimentology, micromorphology, and spatial analysis. Microfaunal remains were used to constrain the dates within an ecological zone, whereas macrofauna was analyzed for taxonomy and taphonomy to examine the source of accumulation and hominin behavior. Technological and typological features of the lithic assemblage were used to characterize lithic production at the site. Materials recovered from Layer 3 in Velika Balanica and from Layer 2 in Mala Balanica, both dated to MIS 9-7, include a distinctive set of archaeological assemblages which resemble contemporaneous Yabrudian assemblages from the Levant in important ways, and which are unlike contemporary material from the surrounding regions. In Velika Balanica, the lithic assemblages are associated with a large fireplace containing evidence of human activities similar to those from Qesem Cave (Israel). Dental remains uncovered in the same layer are consistent with Neanderthals. These findings suggest that the end of the Middle Pleistocene (before 300-240 ka) saw population movement and/or cultural transmission between Southwest Asia and the Balkans, which led eventually to a transfer of technology between Middle Eastern and European hominin populations and contributed to the shaping of Neanderthal behaviors throughout the eastern and northern Mediterranean.

The evolution and changing ecology of the African hominid oral microbiome.

The oral microbiome plays key roles in human biology, health, and disease, but little is known about the global diversity, variation, or evolution of this microbial community. To better understand the evolution and changing ecology of the human oral microbiome, we analyzed 124 dental biofilm metagenomes from humans, including Neanderthals and Late Pleistocene to present-day modern humans, chimpanzees, and gorillas, as well as New World howler monkeys for comparison. We find that a core microbiome of primarily biofilm structural taxa has been maintained throughout African hominid evolution, and these microbial groups are also shared with howler monkeys, suggesting that they have been important oral members since before the catarrhine-platyrrhine split ca. 40 Mya. However, community structure and individual microbial phylogenies do not closely reflect host relationships, and the dental biofilms of Homo and chimpanzees are distinguished by major taxonomic and functional differences. Reconstructing oral metagenomes from up to 100 thousand years ago, we show that the microbial profiles of both Neanderthals and modern humans are highly similar, sharing functional adaptations in nutrient metabolism. These include an apparent Homo-specific acquisition of salivary amylase-binding capability by oral streptococci, suggesting microbial coadaptation with host diet. We additionally find evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that is not observed in later modern human populations. Differences in the oral microbiomes of African hominids provide insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.

The first Neanderthal specimen from Serbia: Maxillary first molar from the Late Pleistocene of Pesturina Cave.

Neanderthals were the only human group in Europe throughout the Late Pleistocene until the arrival of modern humans, and while their presence has been confirmed in the surrounding regions, no Neanderthal fossils are known to date from the Central Balkans. Systematic excavations of Pesturina Cave (Serbia) resulted in the discovery of a permanent right M1 (Pes-3). The specimen was recovered from stratigraphic Layer 4b with an estimated age of 102.4 ± 3.2 ka, associated with Mousterian artifacts. The exceptional state of preservation and minimal wear of the molar enabled a detailed description and comparative analysis of the inner and outer dental structure, including non-metric dental traits and morphometric features of the crown, roots, and dental tissues. The results of this study strongly support the identification of Pes-3 as Neanderthal. Non-metric traits of the occlusal surface of the crown, enamel-dentine junction, and roots are consistent with Neanderthal morphology. The crown shows morphometric features typical for Neanderthal M1, such as a buccolingually skewed crown shape, internally compressed cusps, and a relatively large hypocone. The specimen also shows Neanderthal-like dental tissue proportions, characterized by relatively thin enamel and large coronal dentine and coronal pulp volumes. The discovery of the Pes-3 molar therefore confirms the presence of Neanderthals in the territory of Serbia and the Central Balkans at the end of Marine Isotope Stage (MIS) 5c.

New radiometric ages for the BH-1 hominin from Balanica (Serbia): implications for understanding the role of the Balkans in Middle Pleistocene human evolution.

Newly obtained ages, based on electron spin resonance combined with uranium series isotopic analysis, and infrared/post-infrared luminescence dating, provide a minimum age that lies between 397 and 525 ka for the hominin mandible BH-1 from Mala Balanica cave, Serbia. This confirms it as the easternmost hominin specimen in Europe dated to the Middle Pleistocene. Inferences drawn from the morphology of the mandible BH-1 place it outside currently observed variation of European Homo heidelbergensis. The lack of derived Neandertal traits in BH-1 and its contemporary specimens in Southeast Europe, such as Kocabas, Vasogliano and Ceprano, coupled with Middle Pleistocene synapomorphies, suggests different evolutionary forces acting in the east of the continent where isolation did not play such an important role during glaciations.

A human mandible (BH-1) from the Pleistocene deposits of Mala Balanica cave (Sicevo Gorge, Nis, Serbia).

Neandertals and their immediate predecessors are commonly considered to be the only humans inhabiting Europe in the Middle and early Late Pleistocene. Most Middle Pleistocene western European specimens show evidence of a developing Neandertal morphology, supporting the notion that these traits evolved at the extreme West of the continent due, at least partially, to the isolation produced by glacial events. The recent discovery of a mandible, BH-1, from Mala Balanica (Serbia), with primitive character states comparable with Early Pleistocene mandibular specimens, is associated with a minimum radiometric date of 113 + 72 - 43 ka. Given the fragmented nature of the hemi-mandible and the fact that primitive character states preclude assignment to a species, the taxonomic status of the specimen is best described as an archaic Homo sp. The combination of primitive traits and a possible Late Pleistocene date suggests that a more primitive morphology, one that does not show Neandertal traits, could have persisted in the region. Different hominin morphologies could have survived and coexisted in the Balkans, the "hotspot of biodiversity." This first hominin specimen to come from a secure stratigraphic context in the Central Balkans indicates a potentially important role for the region in understanding human evolution in Europe that will only be resolved with more concentrated research efforts in the area.